Better Understanding The Impact Of Deoxynivalenol On Rainbow Trout

The future growth and sustainability of the aquaculture industry depends on the ability of the sector to identify economically viable and environmentally-friendly alternatives to marine-derived ingredients. In the last few years, the industry has been concentrating its efforts on finding alternative sources of protein to substitute fishmeal in aquafeeds.

Consequently, many new alternatives are available, e.g. insect meal, macroalgae meal, or single-cell protein. However, high costs and limited availability are still challenges to overcome with these novel alternative protein sources. Plant-based meals seem to be one of the most promising and viable solutions, but a common problem that arises from the use of plant ingredients is the presence of mycotoxins.

Mycotoxins are toxic secondary metabolites produced by molds, which can be produced on agricultural commodities before and/or after harvest, during transportation or storage. Mycotoxins are a significant problem worldwide, causing adverse health outcomes when consumed by humans and animals and are responsible for significant economic losses worldwide due to condemned agricultural products. Deoxynivalenol (DON) is one of the more than 400 mycotoxins identified so far. DON is produced by Fusarium fungi, which are generally produced in the field rather than in storage conditions. This means that DON is conveyed from plant-based raw materials used to produce aquafeeds, as mycotoxins commonly occurring in plantstuffs are not destroyed during most processing operations.

The toxic effects of DON — a mycotoxin commonly known as “vomitoxin” as it causes vomiting in livestock — is well described including clinical symptoms for land farmed animals, however, very little is known for aquatic animals. In the case of DON ingestion in fish, no known distinct subclinical signs of DON toxicoses (i.e. no distinct lesions/pathologies) are described, except the accentuated anorexia and decrease in feed intake. In order to understand the reasons behind the lack of clinical manifestation, the aim of the work was to evaluate and elucidate the impact of DON on rainbow trout by exploring new tools and evaluating new diagnostic factors, which may be used later by the industry as standards to better diagnose mycotoxicoses in fish.

At the executed experiment, an accentuated reduction of growth performance was observed after trout were fed DON (4,714 ± 566 and 11,412 ± 1,141 µg/kg). Between many other results, was observed that despite the accentuated anorexia, especially at the higher exposure level of DON (Figure 1), no macroscopic lesions were found (e.g. internal or external hemorrhages, dermal and oral lesions, abnormal pigmentation, or damage to fins). This confirms that a diagnosis of DON ingestion is extremely difficult to be evaluated at the farm level, which can lead to severe economic losses at the farm level.

Authors observed that DON contamination seems to affect essential amino acid digestibility. In the present study, it was observed that DON affected trypsin, and consequently, trypsin may influence the levels of insulin, which will ultimately influence amino acid uptake. The influence of DON at this pathway may influence directly the decrease of growth performance.

The decrease in feed intake was also elucidated at the present work and adenylate cyclase-activating polypeptide (PACAP), a neuroendocrine satiety regulator, seems to be influenced by the ingestion of DON. PACAP plays an important and direct role in the regulation of feed intake and its upregulation of trout’s fed DON provides a possible link to the observed reduction in feed intake. Moreover, PACAP greatly decreases the frequency of gut motility waves, which might also have an impact on nutrient absorption.

The most curious aspect of DON intake is the lack of symptoms, especially when comparing to the livestock species also affected by the ingestion of DON. In the present study, it has been shown for the first time in rainbow trout that DON is metabolized into DON-3-sulfate, which is less toxic than DON. The formation of DON-3-sulfate can help to explain the absence of major clinical signs in trout fed DON, as the exposure to DON is minimized.

It was observed that the ingestion of DON decreases the activity of trypsin significantly, which seems to have a direct influence on the levels of insulin, which ultimately will influence the amino acid uptake. Suppression of appetite due to DON ingestion and observable by the increased gene expression of PACAP might be a defense mechanism in order to decrease the exposure of the animal to DON, therefore reducing the potential negative impacts of DON. Moreover, the biotransformation of DON into DON-3-sulfate minimizes the exposure of the gastrointestinal tract to the potential toxicological effect of DON, helping also to explain the lack of symptoms on animals fed DON.

The discovery of DON-3-sulfate as a novel trout metabolite makes it a potential biomarker of DON exposure, helping farmers to better diagnose the ingestion of DON.

Figure 1: Rainbow trout’s visual differences in growth between the three dietary treatments (Control, 4,714 ± 566 and 11,412 ± 1,141 µg/kg, from left to right). Fish shown in the figure are examples of the growth difference found in the different experimental groups. No clinical signs are observed, except the accentuated anorexia in DON 11 (far right). Credit: Rui A. Goncalves

These findings are described in the article entitled Impact of deoxynivalenol on rainbow trout: Growth performance, digestibility, key gene expression regulation and metabolism, recently published in the journal Aquaculture.

This work was conducted by Rui A. Gonçalves, Carmen Navarro-Guillén, Neda Gilannejad, Jorge Dias, Dian Schatzmayr, Gerlinde Bichl, Tibor Czabany, Francisco Javier Moyano, Paulo Rema, Manuel Yúfera, Simon Mackenzie, and Gonzalo Martínez-Rodríguez from BIOMIN Holding GmbH, Instituto de Ciencias Marinas de Andalucía, PAROS Lda., the University of Stirling, the Universidad de Almería, and the Universidade de Trás-os-Montes e Alto Douro.